… he did believe in the inheritance of certain “acquired characters”—the effects of the conditions of life and of use and disuse.

Though Darwin had been careful to use the terms use and disusedescriptively in Origin of Species, Huxley took them as categorically Lamarckian, a separate alternative to natural selection that did not mingle with it.

Ernst Mayr also presented Darwin’s thinking about use and disuse as singularly Lamarckian, in support of which he quoted from Origin of Species (1859: 134):

There can be little doubt that use in our domestic animals strengthens and enlarges certain parts and disuse diminishes them; and that such modifications are inherited.

Underscoring his Lamarckian take on Darwin, Mayr adds (1982: 691):

Use and disuse, of course, is of importance only if one believes in an inheritance of acquired characters. This Darwin affirms repeatedly … Darwin is quite positive: “Modifications [caused by use and disuse] are inherited.”

Standing alone, the sentence Mayr quotes from Origin of Species looks like a Lamarckian match. With each step back to see it in context, the resemblance fades.

In the next sentence, Darwin (1859: 134) refers to “… the effects of long-continued use and disuse,” not one generation to the next.

In the same paragraph he places use and disuse in the situation of stable selection pressures, offering as examples the “… wingless condition of several birds, which … inhabited several oceanic islands tenanted by no beasts of prey.”

On the next page he explicitly rejects Lamarckian inheritance of mutilations.

On the following page he clarifies “long-continued,” referring to “thousands of successive generations.”

And throughout Origin of Species, Darwin uses “acquired” only in reference to species across many generations in the context of specific selection pressures, not in the Lamarckian sense of individuals transmitting from one generation to the next characteristics acquired during their lifetimes.

In context, the “domestic animals” Darwin drew to our attention were domesticated species, not his neighbor’s individual dogs. Darwin saw species acquiring traits that became heritable when long-continued activities shaped selection pressures.

Jean Gayon repeated Mayr’s Lamarckian misreading of the identical quote from Origin of Species a decade later (1998 [1992]: 150).

Gayon is in the good company of many besides Huxley and Mayr. Science educators bemoan their failure to convince students that natural selection “does not involve effort, trying, or wanting” or “organisms trying to adapt” (Understanding Evolution, 2014). When their students accurately intuit that evolution has produced animals capable of effortful adaptation and these efforts can affect selection processes, this is considered “a significant departure from a scientific understanding of how animals change via natural selection” (Kelemen 2012: 71).

Huxley, Mayr, Gayon and science teachers stumbled over that ordinary and useful habit of thought, categorizing, while overlooking Darwin’s earnest doubts about the categories of his cultural inheritance (Beer 2009: xxx). The terms use and disusegrew into their common biological usage during the Lamarckian half-century that preceded Origin of Species. While Darwin was growing up, they acquired conceptual, social and political significance beyond concrete reference to specific animal activities. For many, the terms were synonymous with Lamarckian inheritance. Lamarckism has been called use-disuse theory.

When Darwin used these terms, he knew the importance of their secondary meanings for his readers. He also recognized the scientific and public relations merits of using these familiar terms for animal behavior in a more descriptive, pared down way.

Scientifically, he advanced more modest claims of animal agency than Lamarckian use of the terms. Darwin’s descriptive use of use and disuse created conceptual space for a developmental view of evolution that was not Lamarckian.

At the same time, Darwin wanted his readers to follow his argument and not give up on it. Pushing against the constraints of traditional terms by using them in nontraditional ways, Darwin’s “generous semantic practice” (Beer 2009: 33) allowed the reader to adjust their own yoke to the terms use and disuse. From his calibrated ambiguity, readers could hear in the text such Lamarckian overtones as their sensibilities favored.

Darwin’s semantic generosity quickened after publication of Origin of Species, as he responded to waves of criticism with a strategic retreat toward inclusiveness. In Variations of Animals and Plants under Domestication (1868), “anything which had been documented and accepted by a fellow scientist was included and assessed” (Vorzimmer 1963: 386). Darwin admitted for discussion a provisional hypothesis of Lamarckian inheritance that he had carefully avoided in Origin of Species. Darlington (1959: 41) complained that during this time “ambiguity … became the mode and standard of Darwin’s expression … which in the end soothed and satisfied the troubled world.”

As he changed successive editions of Origin of Species – to his wife Emma’s delight, adding “the Creator” in the second edition – Darwin remained committed to respectful, empirical inquiry that doubled as good public relations for his theory.

While molecules eclipsed the behavior and development of whole organisms in 20th century evolutionary thought, accounts from Darwin’s vantage point persisted. Nobel physicist Erwin Schrödinger (1944: 113) echoed Darwin most clearly.

You simply cannot possess clever hands without using them for obtaining your aims… You cannot have efficient wings without attempting to fly… Selection would be powerless in ‘producing’ a new organ if selection were not aided all along by the organism’s making appropriate use of it….

Joining Huxley at Chicago’s centennial celebration of Origin of Species, Conrad Waddington (1959: 1636) presented a model of evolution that included animal choices.

Thus the animal by its behavior contributes in a most important way to determining the nature and intensity of the selective pressures which will be exerted on it.

Changes in either the environment or an organism’s behavior can alter selection pressure. This places behavioral change on an equal footing with environmental change as a potential cause of evolutionary change … but despite the intuitive appeal of this idea, it remains largely unacknowledged in current evolutionary theory.